Abstract
Coral reef ecosystems have great economic, social, and ecological value. The ecological success of coral reef ecosystems critically depends on coral-algal symbiosis and coral-prokaryotic partnership. However, seasonal changes underlying these relationships in subtropical hard corals of Hong Kong are poorly studied. Here, we compared the community changes of algal symbionts and prokaryotic partners in Platygyra carnosa and Galaxea fascicularis from Hong Kong collected at two seasonal time points of winter and summer via massively parallel sequencing of genetic markers and multivariate analysis. The results indicated that algal symbionts showed no significant changes between the two seasonal time points but prokaryotic partners changed substantially. Prokaryotic partners putatively involved in photosynthesis, nitrogen fixation, and sulfur oxidation increased significantly from winter to summer, while prokaryotic partners potentially associated with chemosynthesis, ammonia oxidation, and nitrite oxidation decreased significantly from winter to summer. Dissolved oxygen and pH served as the main contributors influencing prokaryotic partners in winter, while temperature, turbidity, and salinity played a dominant role in shaping prokaryotic partners in summer. The findings of the present study suggest that season structures prokaryotic partners but not algal symbionts in subtropical hard corals.
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References
Arif C, Daniels C, Bayer T, Banguera-Hinestroza E, Barbrook A, Howe CJ, LaJeunesse TC, Voolstra CR (2014) Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol Ecol 23:4418–4433. https://doi.org/10.1111/mec.12869
Bartram AK, Lynch MD, Stearns JC, Moreno-Hagelsieb G, Neufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Appl Environ Microbiol 77:3846–3852. https://doi.org/10.1128/AEM.02772-10
Behrendt L, Larkum AW, Norman A, Qvortrup K, Chen M, Ralph P, Sorensen SJ, Trampe E, Kuhl M (2011) Endolithic chlorophyll d-containing phototrophs. ISME J 5(6):1072–1076. https://doi.org/10.1038/ismej.2010.195
Cai L, Tian RM, Zhou G, Tong H, Wong YH, Zhang W, Chui APY, Xie JY, Qiu JW, Ang PO, Liu S, Huang H, Qian PY (2018) Exploring coral microbiome assemblages in the South China Sea. Sci Rep 8:2428. https://doi.org/10.1038/s41598-018-20515-w
Cai L, Ye L, Tong AH, Lok S, Zhang T (2013) Biased diversity metrics revealed by bacterial 16S pyrotags derived from different primer sets. PLoS One 8:53649. https://doi.org/10.1371/journal.pone.0053649
Cai L, Zhou G, Tian RM, Tong H, Zhang W, Sun J, Ding W, Wong YH, Xie JY, Qiu JW, Liu S, Huang H, Qian PY (2017) Metagenomic analysis reveals a green sulfur bacterium as a potential coral symbiont. Sci Rep 7:9320. https://doi.org/10.1038/s41598-017-09032-4
Cantin NE, van Oppen MJH, Willis BL, Mieog JC, Negri AP (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405–414. https://doi.org/10.1007/s00338-009-0478-8
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Chen CP, Tseng CH, Chen CA, Tang SL (2011) The dynamics of microbial partnerships in the coral Isopora palifera. ISME J 5:728–740. https://doi.org/10.1038/ismej.2010.151
D'Angelo C, Hume BC, Burt J, Smith EG, Achterberg EP, Wiedenmann J (2015) Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/Arabian Gulf. ISME J 9:2551–2560. https://doi.org/10.1038/ismej.2015.80
Goodkin NF, Switzer AD, McCorry D, DeVantier L, True JD, Hughen KA, Angeline N, Yang TT (2011) Coral communities of Hong Kong: long-lived corals in a marginal reef environment. Mar Ecol Prog Ser 426:185–196. https://doi.org/10.3354/meps09019
Gordon BR, Leggat W (2010) Symbiodinium-invertebrate symbioses and the role of metabolomics. Mar Drugs 8:2546–2568. https://doi.org/10.3390/md8102546
Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methe B, DeSantis TZ, Human Microbiome C, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504. https://doi.org/10.1101/gr.112730.110
Hammer Ø, Harper DAT, Ryan DR (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9pp
Krediet CJ, Ritchie KB, Paul VJ, Teplitski M (2013) Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. P Roy Soc B-Biol Sci 280:20122328. https://doi.org/10.1098/rspb.2012.2328
LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134. https://doi.org/10.2307/1542872
Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
Lee OO, Yang JK, Bougouffa S, Wang Y, Batang Z, Tian RM, Al-Suwailem A, Qian PY (2012) Spatial and species variations in bacterial communities associated with corals from the Red Sea as revealed by pyrosequencing. Appl Environ Microbiol 78:7173–7184. https://doi.org/10.1128/AEM.01111-12
Lema KA, Willis BL, Bourne DG (2014) Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the Acropora millepora microbiome. Environ Microbiol 16:3345–3359. https://doi.org/10.1111/1462-2920.12366
Li J, Chen Q, Long LJ, Dong JD, Yang J, Zhang S (2014) Bacterial dynamics within the mucus, tissue and skeleton of the coral Porites lutea during different seasons. Sci Rep 4:7320. https://doi.org/10.1038/srep07320
Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233. https://doi.org/10.1016/S0921-8009(99)00009-9
Morton B (1994) Hong Kong’s coral communities: status, threats and management plans. Mar Pollut Bull 29:74–83. https://doi.org/10.1016/0025-326X(94)90429-4
Pantos O, Bongaerts P, Dennis PG, Tyson GW, Hoegh-Guldberg O (2015) Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix. ISME J 9:1916–1927. https://doi.org/10.1038/ismej.2015.3
Peixoto RS, Rosado PM, Leite DC, Rosado AS, Bourne DG (2017) Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front Microbiol 8:341. https://doi.org/10.3389/fmicb.2017.00341
Pettay DT, Wham DC, Smith RT, Iglesias-Prieto R, LaJeunesse TC (2015) Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc Natl Acad Sci U S A 112:7513–7518. https://doi.org/10.1073/pnas.1502283112
Polidoro B, Carpenter K (2013) Dynamics of coral reef recovery. Science 340:34–35. https://doi.org/10.1126/science.1236833
Rädecker N, Pogoreutz C, Voolstra CR, Wiedenmann J, Wild C (2015) Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol 23:490–497. https://doi.org/10.1016/j.tim.2015.03.008
Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10. https://doi.org/10.3354/meps243001
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362. https://doi.org/10.1038/nrmicro1635
Sharp KH, Pratte ZA, Kerwin AH, Rotjan RD, Stewart FJ (2017) Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata. Microbiome 5:120. https://doi.org/10.1186/s40168-017-0329-8
Stat M, Gates RD (2011) Clade D Symbiodinium in scleractinian corals: a “nugget” of hope, a selfish opportunist, an ominous sign, or all of the above? J Mar Bio 2011:730715. https://doi.org/10.1155/2011/730715
Thompson JR, Rivera HE, Closek CJ, Medina M (2014) Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front Cell Infect Microbiol 4:176. https://doi.org/10.3389/fcimb.2014.00176
Tong H, Cai L, Zhou G, Yuan T, Zhang W, Tian R, Huang H, Qian PY (2017) Temperature shapes coral-algal symbiosis in the South China Sea. Sci Rep 7:40118. https://doi.org/10.1038/srep40118
Wong JCY, Thompson P, Xie JY, Qiu JW, Baker DM (2016) Symbiodinium clade C generality among common scleractinian corals in subtropical Hong Kong. Reg Stud Mar Sci 8:439–444. https://doi.org/10.1016/j.rsma.2016.02.005
Xie JY, Wong JC, Dumont CP, Goodkin N, Qiu JW (2016) Borehole density on the surface of living Porites corals as an indicator of sedimentation in Hong Kong. Mar Pollut Bull 108:87–93. https://doi.org/10.1016/j.marpolbul.2016.04.055
Yang SH, Tseng CH, Huang CR, Chen CP, Tandon K, Lee STM, Chiang PW, Shiu JH, Chen CA, Tang SL (2017) Long-term survey is necessary to reveal various shifts of microbial composition in corals. Front Microbiol 8:1094. https://doi.org/10.3389/fmicb.2017.01094
Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614–620. https://doi.org/10.1093/bioinformatics/btt593
Zhang Y, Yang Q, Ling J, Van Nostrand JD, Shi Z, Zhou J, Dong J (2016) The shifts of diazotrophic communities in spring and summer associated with coral Galaxea astreata, Pavona decussata, and Porites lutea. Front Microbiol 7:1870. https://doi.org/10.3389/fmicb.2016.01870
Zhou G, Cai L, Li Y, Tong H, Jiang L, Zhang Y, Lei X, Guo M, Liu S, Qian PY, Huang H (2017) Temperature-driven local acclimatization of Symbiodinium hosted by the coral Galaxea fascicularis at Hainan Island, China. Front Microbiol 8:2487. https://doi.org/10.3389/fmicb.2017.02487
Acknowledgements
The authors would like to thank Drs. Yue Him Wong, Apple Pui Yi Chui, and James Y. Xie for their kind help in experimental design and field sample collection.
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This study was supported by the NSFC-Guangdong Joint Fund (U1301232).
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Corals are marine invertebrates. The authors declare that this article follows the guidelines established by the Agriculture, Fisheries and Conservation Department of Hong Kong SAR Government.
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Cai, L., Zhou, G., Tong, H. et al. Season structures prokaryotic partners but not algal symbionts in subtropical hard corals. Appl Microbiol Biotechnol 102, 4963–4973 (2018). https://doi.org/10.1007/s00253-018-8909-5
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DOI: https://doi.org/10.1007/s00253-018-8909-5